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On growth and form of the distal air exchange surfaces within the lung

David Warburton, Clarence Wigfall, Harvey Pollack, David Koos, Denise AlAlam, Gianluca Turcatel, Wei Shi, Scott Fraser, Rex Moats
doi: https://doi.org/10.1101/141168
David Warburton
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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  • For correspondence: dwarburton@chla.usc.edu
Clarence Wigfall
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Harvey Pollack
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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David Koos
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Denise AlAlam
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Gianluca Turcatel
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Wei Shi
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Scott Fraser
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Rex Moats
The Saban Research Institute, Children’s Hospital Los Angeles and the Keck School of Medicine and the Dornsife School of Letters, Arts and Sciences of the University of Southern California.
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Abstract

Herein we show, using several novel imaging and computational approaches, how the air exchange units (AEUs) of the lung develop from the tips and sides of distinct families of tortuous ducts, that themselves ramify as distinct families distal to the bronchoalveolar duct junctions (BADJs), prenatally in humans but postnatally in mice. The mature AEUs thus consist of indented spheroids tightly packed between quite regularly spaced distal ducts. Since the diameter of the BADJs and the distal ducts increases rather than decreasing during the formation of AEUs, we further deduce that the AEUs must form by circular epithelial precursor buckling at their mouths with resulting extrusion of their lumen into the surrounding mesenchyme, stabilized firstly by interlocking rings of elastin and later by rings of elastin and collagen fibers surrounding the mouth of each of the prospective AEUs. Furthermore, we show that the surface of each of the AEUs is highly rugose, being indented by the capillary network that lies close beneath the AES membranes. We propose that, the kissing theorem proposed of Newton that expresses the number of times billiard balls may touch within their frame is a parsimonious solution to achieving optimum packing of the distal AES unit spaces, while allowing sufficient space between them to allow for conducting airways, closely applied pulsatile capillary blood vessels, lymphatics, nerves and other key components of the interstitial mesenchyme.

Summary statement Employing novel imaging and computational approaches we here deduce some new concepts as to how the distal shaping of airway lineage stem and progenitor cells may contribute to the growth and form of the air exchange surface (AES) of the lung, distal to the bronchoalveolar duct junction (BADJ). We then propose that the AES extrudes from the sides and tips of distinct families of small ducts, apparently by buckling of the thinning luminal epithelium into the surrounding mesenchyme, stabilized firstly by rings of elastin and later by rings of collagen and elastin fibers, that surround the mouth of each distal unit of the AES. We propose this mechanism as a parsimonious solution to achieving the optimum form, packing density and functional efficiency of the AES, while allowing sufficient space between for the plumbing of conducting airways, pulsatile capillary blood vessels, lymphatics, nerves and other key matrix and cellular components within the interstitial mesenchyme.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted May 23, 2017.
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On growth and form of the distal air exchange surfaces within the lung
David Warburton, Clarence Wigfall, Harvey Pollack, David Koos, Denise AlAlam, Gianluca Turcatel, Wei Shi, Scott Fraser, Rex Moats
bioRxiv 141168; doi: https://doi.org/10.1101/141168
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On growth and form of the distal air exchange surfaces within the lung
David Warburton, Clarence Wigfall, Harvey Pollack, David Koos, Denise AlAlam, Gianluca Turcatel, Wei Shi, Scott Fraser, Rex Moats
bioRxiv 141168; doi: https://doi.org/10.1101/141168

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